© 2008 The Authors Entomologia Experimentalis et Applicata 128: 49–56, 2008
Journal compilation © 2008 The Netherlands Entomological Society 49
DOI: 10.1111/j.1570-7458.2008.00740.x
Blackwell Publishing Ltd
Role of prey–host plant associations on
Harmonia axyridis
and
Episyrphus balteatus
reproduction and predatory efficiency
Ammar Alhmedi, Eric Haubruge & Frédéric Francis*
Functional and Evolutionary Entomology, Gembloux Agricultural University, Passage des Déportés 2, B-5030 Gembloux, Belgium
Accepted: 8 April 2008
Key words:host preference, integrated pest management, Coleoptera, Coccinellidae, Diptera,
Syrphidae, aphids, wheat, green pea, stinging nettle, hoverflies, ladybirds, tritrophic interactions, spatial distribution
Abstract
In order to predict possible locations of Harmonia axyridis Pallas (Coleoptera: Coccinellidae) andEpisyrphus balteatus DeGeer (Diptera: Syrphidae) in the field, we studied their oviposition and prey
preferences in relation to several host plant–prey associations under laboratory conditions.
Oviposi-tion preference of H. axyridis and E. balteatus females was determined for three aphid (Homoptera:
Aphididae)–host plant associations: Microlophium carnosum Buckton on stinging nettle [Urtica dioica
L. (Urticaceae)], Acyrthosiphon pisum Harris on green pea [Pisum sativum L. (Fabaceae)], and
Sitobion avenae F. on wheat [Triticum aestivum L. (Poaceae)]. Prey preference of H. axyridis and
E. balteatus larvae was determined with the aphids M. carnosum, A. pisum, and S. avenae.
Harmonia axyridis females showed a strong oviposition preference for the stinging nettle–
M. carnosum association. The preferred association for ovipostion by E. balteatus was pea-hosting
A. pisum, on which fecundity was also highest. Feeding behaviour was less restricted in H. axyridis,
in which the preferred preys were M. carnosum and S. avenae. A lower specificity of predation was
observed in E. balteatus larvae with respect to A. pisum. These laboratory experiments may help us
to understand the spatial distribution of H. axyridis and E. balteatus in the field.
Introduction
In agroecosystems, the spatial distribution of insect species is determined to a large extent by the oviposition behavior of females, if their larvae have limited dispersal capabilities (Huignard et al., 1986; Hanks, 1999). Oviposition behavior is central to many aspects of insect biology, for example, population dynamics and biological control. Female insects may show a preference for specific host plants as oviposition sites. Such a preference can be influenced by various factors. For example, oviposition preference can be determined by experiences of the female as a larva. This has been demonstrated in some species (Jermy et al., 1968), but not in others (Holopainen, 1989; Ntonifor et al., 1996). Oviposition preference may also be influenced by early adult experience (Traynier, 1984; Jaenike, 1990; Turlings et al., 1993), as experience on a previous host may affect
fertility on a subsequent host (Jaenike, 1990; Cunningham et al., 1998). Other factors influencing oviposition preference are competition for sites (Finch & Jones, 1987; Jaenike, 1990; Dicke, 2000), presence of natural enemies (Root, 1973; Ohsaki & Sato, 1994; Dicke, 2000), and distribution of potential host plants (Wiklund, 1982; McLain, 1992; Päts et al., 1997). There is little information about how generalist predators, such as the aphidophagous
multi-coloured Asian ladybird Harmonia axyridis Pallas (Coleoptera:
Coccinellidae) and the hoverfly Episyrphus balteatus DeGeer
(Diptera: Syrphidae), decide which kind of prey to consume. Most insects are rather specific when choosing their food (Hodek, 1993; Schoonhoven et al., 1998), and even generalist predators display a hierarchy of preferences for different hosts (Sadeghi & Gilbert, 1999).
Optimal foraging theory assumes that predators select prey in order to maximize their fitness through optimal choices based on the caloric and nutritive value of prey and associated foraging costs (Stephen & Krebs, 1986). Several *Correspondence: E-mail: francis.f@fsagx.ac.be
50 Alhmedi et al.
factors affect prey selection: (i) prey features, such as species (Molles & Pietruszka, 1987; Roger et al., 2000), size (Allan et al., 1987; Roger et al., 2000), mobility (Clements & Harmsen, 1990; Eubanks & Denno, 2000), nutritional quality (Houck, 1991; Eubanks & Denno, 2000), and population density (Jeschke & Tollrian, 2000); and (ii) predator characteristics, such as size (Allan et al., 1987; Erickson & Morse, 1997), age (Sullivan, 1984; Cisneros & Rosenheim, 1997), and feeding state (e.g., Molles & Pie-truszka, 1987; Houck, 1991).
Harmonia axyridis is used as a control agent against aphid
populations, because its larvae are voracious, polyphagous, and easy to rear (Ferran et al., 1996; Koch, 2003). As an adult, it is known to have strong dispersal capacities (Osawa, 2000; Koch, 2003) and studies in North America have shown that it can rapidly colonize large areas (Tedders & Schaefer, 1994). In Europe, it has spread very rapidly, particularly since 2002, and feral populations of the species now exist in 13 European countries (Brown et al., 2007). Since 1999, the Belgian Ladybird Working Group has mapped all Belgian Coccinellidae and recorded data on
substratum plants and habitat. The first feral H. axyridis
population in Belgium was recorded in 2001, but it has now colonized the whole country. Recorded occupancy in Belgium showed an average rate of increase of 189% between 2002 and 2006 (Adriaens et al., 2008). Laboratory
experiments showed that H. axyridis is frequently involved
in intraguild interactions with other aphidophagous
species, such as the ladybird species Adalia bipunctata (L.)
and Coccinella septempunctata L., both native to western
Europe (Hironori & Katsuhiro, 1997; Cottrell & Yeargan, 1998; Yasuda et al., 2001). In a previous field study, where
Microlophium carnosum Buckton, Sitobion avenae F., and
Acyrthosiphon pisum Harris (all Homoptera: Aphididae) were
the main aphids recorded in high numbers on stinging nettle, wheat, and pea, respectively, a spatial distribution
for H. axyridis was found: throughout the observation
period, it was most abundant on stinging nettle, less in a pea crop, and absent from a wheat field (Alhmedi et al., 2007). Several factors may have an impact on the oviposition behavior of aphidophagous ladybirds, such as (i) aphid species (Blackman, 1967; Olszak, 1988; Kalushkov & Hodek, 2004; Provost et al., 2006), (ii) aphid density (Dixon, 1959), (iii) aphid colony age (Dixon, 2000), and (iv) presence of intra- or inter-specific competitors/predators (Mills, 1982; Osawa, 1993; Burgio et al., 2002). Many experi-ments have demonstrated that aphids are not all equally suitable for the larval growth or adult reproduction of a particular ladybird species (Blackman, 1967; Olszak, 1988;
Kalushkov & Hodek, 2004). For example, C. septempunctata
adults respond differently to the kairomones produced by different aphid species (Sengonca & Liu, 1994). This indicates
that females may be able to discriminate between aphid species. If this is the case, females should lay eggs more readily near suitable than moderately suitable or unsuitable aphids.
The larvae of many hoverfly species, such as the common
hoverfly E. balteatus, are also important natural enemies of
aphids (Chambers & Adams, 1986; Tenhumberg, 1995).
While E. balteatus larvae feed on a wide variety of aphid
species, even within a single habitat (e.g., Mizuno et al., 1997),
there are clear indications of host preferences. Episyrphus
balteatus is recorded as being more generalized than other
syrphids, such as Syrphus ribesii (e.g., Ninomyia, 1957),
but typically this species is found in various prey colonies within one habitat (Wnuk, 1972; Mizuno et al., 1997). In the present study, we investigate oviposition and predation
preference of H. axyridis and E. balteatus in relation to host
plant–prey associations.
Materials and methods
Plant and insect materials
All aphidophagous predators, aphids, and host plants used
in our tests were cultured and reared at 22 ± 2 °C and at
L16:D8 photoperiod. Similar climatic conditions were used for all experiments. Culture medium for plant growth consisted of a mix of vermiculite and perlite. Broad bean
plants were sown in pots (12 cm in diameter × 10 cm high;
9 seeds per pot) in a culture room. The broad bean aphid,
Megoura viciae Buckton, mass-reared on potted broad bean
in the laboratory, was used as prey for the predator cultures. Wheat, pea, and stinging nettle plants were grown in
pots (12 cm in diameter × 10 cm high) in a rearing room,
and used as host plants for the three aphid species in the oviposition preference experiments. A culture of the cereal
aphid, S. avenae, obtained from the Walloon Center of
Agronomic Research of Gembloux, was established on
potted wheat. The pea aphid, A. pisum, reared on broad
bean plants in the laboratory, was established on potted
green pea. The stinging nettle aphid, M. carnosum, was
collected from a natural area of nettle in Gembloux and cultured on potted stinging nettle in the laboratory. The aphids mentioned here were the main aphid species recorded on nettle, pea, and wheat in fields (Alhmedi et al., 2007).
Multicoloured Asian ladybird adults, H. axyridis, were
obtained from Eric Lucas’ laboratory in Montreal, Canada,
reared in an incubator for several generations, at 22 ± 2 °C
and L16:D8 photoperiod, and provided with bee-collected pollen, crystalline sugar, and water. Pollen and water were changed once per week and egg batches were collected
regularly. Adults and larvae were fed with M. viciae aphids
and reared on broad bean leaves and pollen in boxes of
Prey–host plant–Harmonia axyridis associations 51
The native hoverfly E. balteatus was cultured in wooden
cages (60 × 100 × 100 cm) with a sliding door. Adults were
maintained in a constant environment of 22 ± 2 °C and
L16:D8 photoperiod, and they were provided with bee-collected pollen, crystalline sugar, and water. Pollen and water were refreshed every 2 days. In the mass culture, adult females were stimulated to oviposit by presenting
pots of broad bean infested with M. viciae. A batch of
eggs that was laid over a 2–3-h period provided a cohort of flies with synchronous larval emergence within 48–
72 h. Emerged larvae were fed with M. viciae cultured on
broad bean.
Oviposition preference of Harmonia axyridis and Episyrphus balteatus Oviposition preference experiments were performed in
the laboratory with 4-week-old adult females of H. axyridis
and E. balteatus. The fertility of all females used was
assessed 3 days prior to the preference test by counting the
eggs laid on pots of broad bean infested with M. viciae.
All H. axyridis (1 day before ovipositional tests) and
E. balteatus females (3 days before ovipositional tests) used
had no previous exposure to aphids. Oviposition preference of adult females was tested in single- and dual-choice experiments. Three aphid/host plant associations (namely,
wheat with S. avenae, pea with A. pisum, and stinging
nettle with M. carnosum; in short ‘plant + aphid’) were
offered. Ten replicates were run simultaneously for each test. Great care was taken to ensure that all replicate plants were the same size and contained the same number of aphids (200 aphids per plant).
Non-choice experiment. One day after the start of aphid
infestation, a single gravid female was introduced into a
plastic bottle (9 cm in diameter × 25 cm high), containing
the potted plant + aphids. Eggs laid after 2 and 24 h were recorded in each replicate.
Dual-choice experiment. One day after the start of aphid
infestation, a single gravid female was introduced into a
cage (25 × 25 × 35 cm), containing two different potted
plants and aphids. Eggs laid after 2 and 24 h were recorded in each replicate.
Predation preference of Harmonia axyridis and Episyrphus balteatus larvae
Second instars of H. axyridis and E. balteatus were starved
overnight before their predation preference was tested in dual-choice experiments, using the three aphid species as prey. Twenty aphid individuals per species were offered in a Petri dish (9 cm in diameter). Ten replicates were run simultaneously for each test. Aphids eaten were recorded after 2, 6, and 24 h.
Statistical analysis
The results of the experiments were analyzed using Minitab 15 and SAS (SAS Institute, 1998). Prior to the analyses, data were checked for equal variances and
normality, and log(n + 1) transformed if necessary.
Oviposition rates of H. axyridis and E. balteatus
females (non-choice) for plant + aphid were analyzed using one-way analysis of variance (ANOVA). Student– Newman–Keuls tests were run to compare the means among treatments. Data on preference were analyzed using χ2
-test.
Results
Oviposition preference of Harmonia axyridis and Episyrphus balteatus
Non-choice experiment. Without an alternative option,
H. axyridis females oviposited more on aphid-infested
nettle than on other plants after 2 h (ANOVA: F2,27 = 11.58,
P<0.001). From 2–24 h after start, egg numbers did not
differ among plants (F2,27 = 2.92, P = 0.071). For E. balteatus,
there was no significant difference (F2,27 = 1.87, P = 0.173)
in the number of eggs laid after 2 h, but from 2–24 h after the start of the experiment more eggs were laid on
aphid-infested pea (F2,27 = 10.33, P<0.001) than on either
aphid-infested wheat or nettle. Overall, H. axyridis
laid more eggs on aphid-infested nettle (F2,27 = 16.61,
P<0.001) than on either aphid-infested wheat or pea,
while E. balteatus laid more eggs on aphid-infested pea
(F2,27 = 10.97, P<0.001) than on either aphid-infested
wheat or nettle (Figure 1).
Dual-choice experiment. After 2 h, H. axyridis females had
laid more eggs on nettle + aphid than on the other plants (χ2
= 56.0 for wheat + aphid; χ2
= 26.0 for pea + aphid; both comparisons: d.f. = 1, P<0.001; Figure 2). From 2–24 h, a similar result was obtained: oviposition was highest on
nettle + aphid (χ2
= 112.8 for wheat + aphid; χ2
= 136.0 for pea + aphid; both comparisons: d.f. = 1, P<0.001). Comparing the two least preferred aphid/host plant combinations, oviposition was lowest on wheat + aphid (after 2 h: χ2
= 6.0, d.f. = 1, P = 0.014; 2–24 h: χ2
= 55.7, d.f. = 1, P<0.001).
Episyrphus balteatus females laid significantly more eggs on aphid-infested pea than on wheat + aphid (after 2 h:
χ2 = 182.0; 2–24 h: χ2
= 384.3; both: d.f. = 1, P<0.001) or
nettle + aphid (after 2 h: χ2
= 148.9; 2–24 h: χ2
= 121.6; both: d.f. = 1, P<0.001). After 2 h, oviposition on wheat
+ aphid and nettle + aphid did not differ (χ2
= 0.02, d.f. = 1, P = 0.881), but from 2–24 h more egges were
laid on wheat + aphid (χ2
= 5.2, d.f. = 1, P = 0.022) (Figure 2).
52 Alhmedi et al.
Predation preference of Harmonia axyridis and Episyrphus balteatus larvae
Overall, the consumption rate of second instars of H. axyridis differed among aphid species: equal numbers
of S. avenae and M. carnosum were consumed (χ2
= 0.4, d.f. = 1, P = 0.548), but fewer of A. pisum (compared with
S. avenae: χ2
= 85.9; with M. carnosum: χ2
= 45.4; both: d.f. = 1, P<0.001). Consumption rates varied among observation intervals, where aphids eaten were counted after 2 h (0–2 h), 6 h (2–6 h), and 24 h (6–24 h) (Figure 3). When M. carnosum and A. pisum were offered simultaneously, H. axyridis larvae ate more M. carnosum than A. pisum during the first and third period of the experiment (after
2 h: χ2 = 13.4; 6–24 h: χ2
= 20.8; both: d.f. = 1, P<0.001). Harmonia axyridis larvae consumed more S. avenae than
M. carnosum during the first and second period (χ2
= 11.5,
d.f. = 1, P = 0.001 and χ2
= 4.5, d.f. = 1, P = 0.034, respectively), but more M. carnosum than S. avenae during the third
period (χ2
= 12.4, d.f. = 1, P<0.001). Ladybird larvae ate consistently more S. avenae than A. pisum (after 2 h:
χ2 = 23.9; 2–6 h: χ2
= 16.4; 6–24 h: χ2
= 26.2; all: d.f. = 1, P<0.001).
Overall, the consumption rate of E. balteatus larvae also differed among aphid species: M. carnosum was eaten most
(compared with S. avenae: χ2
= 14.4, d.f. = 1, P<0.001) and equal numbers of S. avenae and A. pisum were consumed Figure 1 Oviposition rate (mean + SE number of eggs) of Harmonia axyridis and Episyrphus balteatus in a non-choice experiment according to host plant–prey association (gray bars represent green pea–Acyrthosiphon pisum association, black bars represent wheat–Sitobion avenae association, and white bars represent stinging nettle–Microlophium carnosum association). Bars capped with the same letter during each observation period are not significantly different (one-way ANOVA and Student–Newman–Keuls test: P<0.05).
Figure 2 Oviposition preference (mean + SE number of eggs) of Harmonia axyridis and
Episyrphus balteatus in a dual-choice experiment for different host plant–prey associations (gray bars represent green pea–Acyrthosiphon pisum association, black bars represent wheat–Sitobion avenae association, and white bars represent stinging nettle–Microlophium carnosum association). Bars capped with the same letter during each observation period are not significantly different (χ2
-test for observed and expected frequencies, null hypothesis: number of eggs laid is equal in all plants: P>0.05).
Prey–host plant–Harmonia axyridis associations 53
(χ2
= 3.8, d.f. = 1, P = 0.050). When M. carnosum and A. pisum were offered in combination, A. pisum was eaten
more during the first 2 h (χ2
= 13.4, d.f. = 1, P<0.001), but
thereafter it was eaten less (from 2–6 h: χ2
= 6.7, d.f. = 1,
P = 0.010; 6–24 h: χ2
= 9.8, d.f. = 1, P = 0.002). During the first and third period, equal numbers of M. carnosum and S. avenae were consumed. Only from 2–6 h, M. carnosum
was eaten more (χ2
= 8.6, d.f. = 1, P = 0.003).
Discussion
When H. axyridis and E. balteatus females had no choice between aphid/host plant combinations, they oviposited on the plants offered. However, these generalist predators displayed significant differences in egg distribution and prey consumption among the various aphid species. This result supports literature data that suggest selectivity of oviposition (Mitchell, 1962; Niemczyk & Pruska, 1986; Budenberg & Powell, 1992). When H. axyridis females were offered a choice, they oviposited preferably on stinging nettle infested with M. carnosum, and least on wheat infested with S. avenae. Similarly, H. axyridis larvae preferred to prey on M. carnosum, whereas pea aphid was least eaten. These preferences of H. axyridis match with our field observation that this predator was found most often on stinging nettle, and (much) less on pea or wheat (Alhmedi et al., 2007).
Differential consumption rate might be indicative of the ability of H. axyridis and E. balteatus larvae to differentiate between aphid species, and also shows differences in aphid palatability, which may be due to differences in morphol-ogy, behavior, and chemical constitution (Okamoto, 1966; Liepert & Dettner, 1996; Dixon, 2000). The oviposition and consumption preference observed in H. axyridis and E. balteatus females and larvae in the present study may be explained by optimal foraging theory, which states that the female is likely to select oviposition sites harboring prey that will best support the development and survival of her progeny (Kindlmann & Dixon, 1993).
Females and larvae of E. balteatus were found to be less specific in comparison with H. axyridis: females preferred A. pisum on pea for oviposition, but larvae preferred M. carnosum for predation. Previous research by Röder (1990) and Torp (1994) reported E. balteatus in equal abundance in all biotypes. This finding also supports field observations by Alhmedi et al. (2007) of similar abundance of E. balteatus in different habitats, in association with the occurrence and abundance of aphids. Sadeghi & Gilbert (1999) found that feeding preferences differed among female E. balteatus, indicating that part of a population may be specialized, whereas the other part may consist of generalist females.
The oviposition and predation preference of H. axyridis observed in the laboratory, as well the specific distribution Figure 3 Prey preference (mean + SE
number of aphid consumed) of Harmonia axyridis and
Episyrphus balteatus for different aphid species (gray bars represent
Acyrthosiphon pisum, black bars represent Sitobion avenae, and white bars represent Microlophium carnosum). Bars capped with the same letter during each observation period are not significantly different (χ2-test for observed and expected frequencies, null hypothesis: number of eggs laid is equal in all plants: P>0.05).
54 Alhmedi et al.
previously recorded in the field (Alhmedi et al., 2007), may help us to understand its invasion of agroecosystems. For example, the introduction of stinging nettle in pest-management strategies, as shelter for important natural enemies, could lead to undesirable increases of the top predator H. axyridis and subsequently enhance the negative interactions with native ladybirds, such as C. septempunctata (Yasuda et al., 2004) and A. bipunctata (Burgio et al., 2005). However, because H. axyridis will likely become perma-nently established in many of the areas it has invaded, we must continue to advance our knowledge on how to reap benefits in situations where H. axyridis is a potential biological control agent and mitigate its effects in situations where it is a potential pest.
In conclusion, although H. axyridis is considered a poly-phagous ladybird, ovipositing females seem to prefer the stinging nettle–M. carnosum complex. Future research is needed to study the orientation of H. axyridis movement from nettle zones toward crop field and vice versa. To this end, a laboratory and field study using kairomones for H. axyridis will be initiated. The aphid alarm pheromone (E)-β-farnesene has already been found to attract C. septempunctata (Al Abassi et al., 2000), A. bipunctata, and E. balteatus (Francis et al., 2001, 2005).
Acknowledgements
We are very grateful to the anonymous reviewers for helpful comments and for English corrections of the manuscript. We thank Prof. Bernard Bodson, Department of Crop Science (FuSaGx) for permission to use the experi-mental field. We are grateful to Yves Brostaux for help with statistical analyses.
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